Surround suppression in mouse auditory cortex underlies auditory edge detection

Surround suppression (SS) is a fundamental property of sensory processing throughout the brain. In the auditory system, the early processing stream encodes sounds using a one dimensional physical space-frequency. Previous studies in the auditory system have shown SS to manifest as bandwidth tuning around the preferred frequency. We asked whether bandwidth tuning can be found around frequencies away from the preferred frequency. We exploited the simplicity of spectral representation of sounds to study SS by manipulating both sound frequency and bandwidth. We recorded single unit spiking activity from the auditory cortex (ACx) of awake mice in response to an array of broadband stimuli with varying central frequencies and bandwidths. Our recordings revealed that a significant portion of neuronal response profiles had a preferred bandwidth that varied in a regular way with the sound's central frequency. To gain insight into the possible mechanism underlying these responses, we modelled neuronal activity using a variation of the Mexican hat function often used to model SS. The model accounted for response properties of single neurons with high accuracy. Our data and model show that these responses in ACx obey simple rules resulting from the presence of lateral inhibitory sidebands, mostly above the excitatory band of the neuron, that result in sensitivity to the location of top frequency edges, invariant to other spectral attributes. Our work offers a simple explanation for auditory edge detection and possibly other computations of spectral content in sounds. Author summaryA central computation performed by the auditory system in the mammalian brain is frequency decomposition. As a result, single neurons throughout the auditory system are often characterized by their preference to basic sound frequencies such as pure tones. Here we tested how single neurons in the mouse auditory cortex respond to sound stimuli with a range of bandwidths around specific central frequencies. We found that single neurons respond strongly to specific bandwidths, and that these responses varied in a regular way based on the sound's central frequency. We could explain the nature of these responses using a simple mathematical model that considers the excitatory central response to frequency and the structure of its inhibitory side bands. We found that some neurons in the auditory cortex are best described by their responses to the location of sharp boundaries, or edges, in the frequency composition of sounds. Taken together, our work highlights aspects of neuronal responses in the mouse auditory cortex that go beyond responses to pure tones.

Automated summary

Surround suppression is a fundamental property of sensory processing in the brain. This study found that there is bandwidth tuning in the auditory system, and proposed a simple explanation for auditory edge detection.